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NOTES ON GEOGRAPHIC DISTRIBUTION Check List 14 (3): 539–544 https://doi.org/10.15560/14.3.539

Ambidexter symmetricus Manning & Chace, 1971 (, ): first record for Rio Grande do Norte and overview of the species distribution on the Brazilian coast

Alex Barbosa de Moraes,1, 4, 5 Daniele Cosme Soares de Moraes,2, 4 Nielson Felix Caetano França,1, 4 Jéssica Medeiros Malheiros,4 Fúlvio Aurélio de Morais Freire1, 2, 3, 4

1 Programa de Pós-Graduação em Sistemática e Evolução, Universidade Federal do Rio Grande do Norte, CEP 59072-970, Natal, RN, Brazil. 2 Programa de Pós-Graduação em Ecologia, Universidade Federal do Rio Grande do Norte, CEP 59072-970, Natal, RN, Brazil. 3 Universidade Federal do Rio Grande do Norte, Centro de Biociências, Departamento de Botânica e Zoologia, CEP 59072-970, Natal, RN, Brazil. 4 Grupo de Estudos em Ecologia e Fisiologia de Animais Aquáticos. Corresponding author. Alex Barbosa de Moraes, [email protected]

Abstract We present the first record of Ambidexter symmetricus Manning & Chace, 1971 for the state of Rio Grande do Norte, northeastern Brazil, filling a distribution gap of this species in the country. We confirm the preference of this species for seagrass meadows in the Curimataú river estuary. Lastly, a brief overview and an updated distribution map for the records of this species on the Brazilian coast are provided.

Key words ; Curimataú river basin; estuary; range extension.

Academic editor: Felipe Bezerra Ribeiro | Received 19 January 2018 | Accepted 25 May 2018 | Published 15 June 2018

Citation: Moraes AB, Moraes DCS, França NFC, Malheiros JM, Freire FAM (2018) Ambidexter symmetricus Manning & Chace, 1971 (Decapoda, Processidae): first record for Rio Grande do Norte and overview of the species distribution on the Brazilian coast. Check List 14 (3): 539–544. https://doi.org/10.15560/14.3.539

Introduction spp.) (Manning and Chace 1971, Lewis 1984, Souza et al. 2011, Pachelle et al. 2016, Rasch and Bauer 2016). This The processid genus Ambidexter Manning & Chace, species has cryptic and nocturnal habits, usually burying 1971 is composed of 3 species worldwide, A. panamensis itself in sandy or muddy soft substrates during the day Abele, 1972, A. swifti Abele, 1972, and A. symmetricus and emerging at night to feed (Manning and Chace 1971, Manning & Chace, 1971, all of which distributed in the Barba et al. 2005). Western Atlantic and Eastern Pacific oceans (Manning Ambidexter symmetricus is the only representative and Chace 1971, Abele 1972, De Grave and Anker 2013). of its genus with an amphi-American distribution; it Ambidexter symmetricus is a small shrimp (maximum car- occurrs in the western Atlantic from Florida (USA) to apace length: 6.7 mm) that commonly occurs in shallow Santa Catarina (Brazil) (Manning and Chace 1971, Abele waters (0–20 m) of coastal and estuarine regions where it 1972, Pachelle et al., 2016), and in the eastern Pacific, inhabits sea grass meadows (Halodule wrightii, Thalas- known only by 1 record in the western Gulf of Califor- sia testudinum, Syringodium filiforme, and Diplanthera nia (Mexico) (Ríos and Carvacho 1982). In Brazil, this

Copyright Moraes et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 540 Check List 14 (3)

Figure 1. Ambidexter symmetricus Manning & Chace, 1971 from the Curimataú River, Rio Grande do Norte, Brazil (GEEFAA/UFRN 890). Lateral view. A. Live adult female. B. Same, antero-lateral view of the cephalothorax showing bifid rostrum. Specimen fixed in 70% ethanol. Scale bar = 1 mm. species has been reported from several localities in the and without occurrence of sea grass, in accordance to states of Ceará, Paraíba, Pernambuco, Espírito Santo, federal environmental laws (Collection license SISBIO- Bahia, Rio de Janeiro, São Paulo, and Santa Catarina IBAMA #28314-1). Digital calipers (0.01 mm accuracy) (Ramos-Porto 1977, Christoffersen 1980, Ramos-Porto were used to measure the length of the carapace of the 1980, Santos and Coelho 1995, Santos and Coelho 1998, specimens (LC, linear distance between the poster orbital Coelho et al. 2006, Nascimento and Torres 2007, Riul et margin and the posterior dorsal margin of the carapace). al. 2008, Souza et al. 2011, Almeida et al. 2012, Amaral The sex of the specimens was determined by the appen- et al. 2010, Terossi and Mantelatto 2014, Pachelle et al. dix masculina on the second pair of pleopods. Finally, 2016). However, many gaps remain throughout the dis- the specimens were fixed in 70% ethanol and deposited tribution of A. symmetricus in Brazil. Thus, we report the in the carcinological collection of the Grupo de Estudos first occurrence record of A. symmetricus in the state of de Ecologia e Fisiologia de Animais Aquáticos, Uni- Rio Grande do Norte, which fills 1 of these distribution versidade Federal do Rio Grande do Norte (GEEFAA/ gaps on the coast of Brazil. UFRN), Brazil. To compare occurrence records of this species at our Methods sites with the presence or absence of marine grass, the homogeneity of data variance and normality were veri- The specimens was collected in the tropical estuarine fied by the Levene and Shapiro-Wilks tests, respectively system of the Curimataú River, which is located on the (Zar 1996). Then, a Wilcoxon’s test (non-parametric southern coast of the state of Rio Grande do Norte, near data) was performed, using the significance level of 5% the border with the state of Paraíba, Brazil. It is within (Zar 1996). the Köppen-Geiger climate region As (Miranda et al. A distribution map was created using the ArcMap 2006, Rubel and Kottek 2010). At sampled site near the 10.1 application of the ESRI ArcGIS™ program pack- mouth of the estuary, the width of the Curimataú River is age using compiled data (Table 1). The list of locations 570 m and the maximum depth varies from 0 to 1.80 m. is based on literature records and our new records. For On both were observed large sandbanks that are exposed at low tide. The substrate of the river is clayey, with a records that were not georeferenced, we estimated geo- predominance of sedimentary fractions of silt and clay graphic coordinates using the Google Earth® (version over most of the area sampled, but shallower areas had 7.1.2.2041). predominantly of sedimentary fractions of fine sand. Throughout the year, the water temperature varyies little, Results approximately 26.6–28.8 °C. The bottom salinity varies Order Decapoda Latreille, 1802 between 29 and 36 ppt (Miranda et al. 2006, A.B. de Moraes personal observation). Infraorder Caridea Dana, 1852 The field samplings were performed at random linear Family Processidae Ortmann, 1896 stretches of 500 m (500 m transects) were along the bor- Genus Ambidexter Manning & Chace, 1971 der of the Curimataú river estuary (between 06°19′25″S, 035°03′08″ W and 06°19′05″ S, 035°02′45″ W). The Ambidexter symmetricus Manning & Chace, 1971 samples were collected with the aid of an artisanal Figure 1 shrimp trawl (12 m × 2 m, 5 mm mesh), in areas with Ambidexter symmetricus Manning and Chace 1971: 3, figs 1, 2. Moraes et al. | Ambidexter symmetricus: first record for Rio Grande do Norte, Brazil 541

Table1. Records of Ambidexter symmetricus Manning & Chace, 1971 in Brazil. Present study highlighted in bold. Geodetic datum = WGS84. * = Records with georeferenced localization estimated based on the description provided on each record.

Location Collection site (state) Latitude Longitude Reference number 1 Corrente Nordeste, Norte do Brasil 01°29’S 039°32’W Coelho Filho 2006* 2 Praia de Requenguela, Banco dos Cajuais (Ceará) 04°40’47”S 037°20’44’’W Pachelle et al. 2016 3 Estuário do rio Curimataú (Rio Grande do Norte) 06°19’10’’S 035°02’45’’W Present study 4 Ponta do Cabo Branco, praia de Cabo Branco (Paraíba) 07°08’50”S 034°47’51”W Riul et al. 2008 5 Canal de Santa Cruz (Pernambuco) 07°44’51”S 034°49’13”W Ramos-Porto 1980* 6 Rio Jaguaribe (Pernambuco) 07°43’S 034°49’W Souza et al. 2011 7 Praia de Pilar (Pernambuco) 07°45’S 034°49’W Souza et al. 2011 8 Praia Forno de Cal (Pernambuco) 07°46’S 034°50’W Souza et al. 2011 9 Rio Paripe (Pernambuco) 07°48’S 034°51’W Souza et al. 2011 10 Banco de areia Ramalho (Pernambuco) 07°49’S 034°49’W Souza et al. 2011 11 Praia de Boa Viagem (Pernambuco) 08°08’S 034°54’W Souza et al. 2011 12 Praia de Boa Viagem (Pernambuco) 08°07’17”S 034°53’41”W Nascimento and Torres 2007 13 Praia de Piedade (Pernambuco) 08°10’S 034°55’W Souza et al. 2011 14 Praia de Candeias e Piedade (Pernambuco) 08°11’19”S 034°54’W Coelho-Santos and Coelho 1998, Souza et al. 2011* 15 Praia de Suape (=Barra Itapoama) (Pernambuco) 08°21’S 034°57’W Souza et al. 2011 16 Maraú, ilha do Tanque (Bahia) 14°00’47.8”S 038°59’00.5”W Almeida et al. 2012* 17 Maraú, Ilha do Tanque (Bahia) 14°00’59”S 038°59’15.6”W Almeida et al. 2012* 18 Praia do Castelhano (Espírito Santo) 20°50’3.24”S 040°37’18.33”W Christoffersen 1980* 19 Praia de Zumbi (Rio de Janeiro) 22°49’12.65”S 043°10’28.44”W Christoffersen 1980* 20 Ilha do Japonês (Rio de Janeiro) 22°52’53.79”S 042°00’17.48”W Christoffersen 1980* 21 Praia Grande (São Paulo) 23°28’19”S 045°03’59”W Christoffersen 1980* 22 Praia do Lamberto (São Paulo) 23°29’46.01”S 045°06’41.53”W Christoffersen 1980* 23 Baía do Araçá (São Paulo) 23°48’55”S 045°24’14”W Amaral et al. 2010* 24 Praia do Araçá (São Paulo) 23°48’S 045°24’W Terossi and Mantelatto 2014, Christoffersen1980 * 25 Baía do Trapandé (São Paulo) 25°02’37”S 047°56’33”W Christoffersen1980 * 26 Praia de Porto Belo (Santa Catarina) 27°09’21”S 048°32’49”W Christoffersen1980 * 27 São José. Praia de Ponta de Baixo (Santa Catarina) 27°38’03”S 048°37’40”W Christoffersen1980 * 28 Ilha de Santa Catarina. Alto Ribeirão (Santa Catarina) 27°42’00”S 048°33’07”W Christoffersen1980 * 29 Praia da Armação (Santa Catarina) 26°47’11”S 048°37’34”W Christoffersen1980 *

New records. Brazil: Rio Grande do Norte: Canguare- 1980, Ríos and Carvacho 1982, Riul et al. 2008, Almeida tama, Curimataú River on marine grass, 06°19′10″ S, and Bezerra 2011, Almeida et al. 2012, Pachelle et al. 035°02′45″ W: 19-V-2017, 3 ♀ ovigerous, CL = 3.9– 2016, this study). 5.2 mm, GEEFAA/UFRN 887; 2 ♀ ovigerous, CL = Identification. Rostrum slightly curved down, not 4.4–5mm), GEEFAA/UFRN 888. 10-I-2017, 8 ♀ (CL extending beyond anterior margin of eye; apex bifid with = 2.7–4.6 mm); 3 ♀ ovigerous (CL = 3.4–4.6 mm), longer lower tooth. Antennal spine present. Stylocerite GEEFAA/UFRN 889, 890. rounded and laterally unarmed. Second pair of pereio- Previous records in Brazil. Northeast Continental Shelf pods symmetrical, with 4 meral articles and 9 or 10 carpal (Coelho Filho 2006), Ceará (Pachelle et al. 2016), Para- articles. Carpus of the fifth pair of pereiopods longer than íba (Riul et al. 2008), Pernambuco (Ramos-Porto 1977, the propodus. Fifth abdominal somite unarmed post- Ramos-Porto 1980, Santos and Coelho 1995, Santos and laterally. Abdominal sternites unarmed. Coelho 1998, Coelho et al. 2006, Nascimento and Torres Color. Body covered with scattered red chromatophores, 2007, Souza et al. 2011), Bahia (Almeida et al. 2012), background semitransparent. Chromatophores arranged Espírito Santo (Christoffersen 1980), Rio de Janeiro in a transverse band on the anterior portion of the abdo- (Christoffersen 1980), São Paulo (Christoffersen, 1980, men. The color is also concentrated in the carapace, Amaral et al. 2010, Terossi and Mantelatto 2014), and pleura and appendages (Fig. 1). Santa Catarina (Christoffersen, 1980) (Table 1). Type locality. Biscayne Bay, Miami, Dade County, Discussion Florida, USA (Manning and Chace 1971). From 56 different points sampled, the most common type Distribution. Western Atlantic: USA (Florida), Gulf of of substrate was sedimentary fractions of silt and clay. Mexico, Caribbean Sea, and Brazil (from Ceará to Santa Despite this, all of specimens collected of A. symmetri- Catarina). Eastern Pacific: Mexico (Gulf of California) cus occurred in areas where marine grass was present (Manning and Chace 1971, Abele 1972, Christoffersen (Wilcoxon test, p <0.001). Specimens of A. symmetricus 542 Check List 14 (3) were also located visually in small pools formed during Barba E, Raz-Guzman A, Sánchez AJ (2005) Distribution pat- the low tide near these areas. These observations agree terns of estuarine caridean shrimps in the southwestern with the ones presented by Manning and Chace (1971) Gulf of Mexico. Crustaceana 78(6): 709-726. https://doi. org/10.1163/156854005774353502 and Rasch and Bauer (2016), who discussed that this spe- Coelho PA, Almeida AO, Souza-Filho JF, Bezerra LEA, Giraldes BW cies is recurrent of marine grass meadows, which makes (2006) Diversity and distribution of the marine and estuarine it an important component of these habitats. However, shrimps (Dendrobranchiata, Stenopodidea and Caridea) from north this species has also been reported from areas having sub- and northeast Brazil. Zootaxa 1221: 41–62. strates formed by calcareous algae (Ramos-Porto 1980), Coelho Filho PA (2006) Checklist of the decapods (Crustacea) from the outer continental shelf and seamounts from northeast of Brazil— biogenic coarse sand (Coelho Filho 2006), sandstone REVIZEE Program (NE III). Zootaxa 1184: 1–27. reefs (Nascimento and Torres 2007), and intertidal rocks Christoffersen ML (1980) Taxonomia e distribuição geográfica dos (Terossi and Mantellato 2014). (Crustacea, Decapoda, Natantia) do Brasil, Uruguai e Pachelle et al. (2016) stated that A. symmetricus is norte da Argentina, incluindo considerações sobre a divisão do sul well-distributed throughout the Brazilian territory, it is do continente em províncias biogeográficas marinhas. PhD thesis, quite rare and difficult to find due to its nocturnal habit. In University of São Paulo, São Paulo, 467 pp. Dana JD (1852) Conspectus crustaceorum, conspectus of the crustacea fact, most Brazilian records in the literature are based on of the exploring expedition under Capt. Wilkes, U.S.N. Macroura. the capture of only 1–3 specimens (Christoffersen 1980, Proceedings of the Academy of Natural Sciences of Philadelphia Coelho and Santos 1988, Coelho Filho 2006, Nascimento 6: 10–28. and Torres 2007, Riu et al. 2008, Almeida et al. 2012, De Grave S, Anker A (2013) New records of processid shrimps from the Pachelle et al. 2016). Indo-West and East Pacific (Crustacea: Decapoda). Zootaxa 3640 Our material represents the first record of this spe- (2): 224–241. https://doi.org/10.11646/zootaxa.3640.2.6 Latreille PA (1802) Histoire naturelle, générale et particulière des crus- cies for the state of Rio Grande do Norte, filling 1 of the tacés et des insects. Tome 6. Paris, pls 44–57391 pp. gaps in the distribution of the species along the Brazilian Lewis FG (1984) Distribution of macrobenthic associated coast. The new sites are located 92 km from the nearest with Thalassia, Halodule and bare sand substrata. Marine Ecology, southern record in Paraíba (Riul et al. 2008) and 375 km Progress Series 19: 101–113. https://doi.org/10.3354/meps019101 from the nearest northern record in Ceará (Pachelle et Manning RB, Chace FA Jr (1971) Shrimps of the family Processidae al. 2016) (Fig. 2). The only records of this species from from the northwestern Atlantic Ocean (Crustacea: Decapoda: Cari- dea). Smithsonian Contributions to Zoology 89: 1–41. https://doi. the states of Espírito Santo, Rio de Janeiro, and Santa org/10.5479/si.00810282.89 Catarina are those collected between 1970 and 1980 and Miranda LB, Bérgamo AL, Ramos e Silva CA (2006) Dynamics of a reported by Christoffersen (1980). tropical estuary: Curimatau River, NE Brazil. Journal of Coastal Research, Special Issue 39 (2): 697–701. Nascimento EF, Torres MFA (2007) Crustáceos decápodos dos recifes Acknowledgements da praia de Boa Viagem, Recife – Pernambuco. Boletim Técnico- We are grateful to the Coordenação de Aperfeiçoamento Científico do CEPENE 15 (1): 43–55. de Pessoal de Nível Superior (CAPES), for the tendered Ortmann, A (1896) Das System der Decapoden-Krebse. Zoologisce Jahrbücer. Abtheilung für Systematik, Geographie und Biologie scholarship to Alex B. de Moraes, Daniele C. S. de Moraes, der Thiere 9: 409–453. Nielson F. C. França and Jéssica M. Malheiros and to the Pachelle PPG, Anker A, Mendes CB, Bezerra LEA (2016) Deca- members of GEEFAA for all the laboratorial support. pod crustaceans from the state of Ceará, northeastern Brazil: an The authors would also like to thank the Programa de Pós updated checklist of marine and estuarine species, with 23 new Graduação em Sistemática e Evolução (UFRN) for the records. Zootaxa 4131 (1): 001–063. https://doi.org/10.11646/ assistance in photographing the specimens. zootaxa.4131.1.1 Ramos-Porto M. (1980) Estudo ecológico da região de Itamaracá, Pernambuco, Brasil. VII Crustáceos Decapodos Natantes. Trabal- Authors’ Contributions hos Oceanográficos da Universidade Federal de Pernambuco 15: 277–310. ABM, DCSM, NFCF, and JMM collected the data, ABM Ramos-Porto M. (1977) Ocorrência de Ambidexter symmetricus Man- identified the , ABM did the taxonomic description, ning & Chace, 1971 no litoral pernambucano. Ciência e Cultura ABM, DCSM, NFCF, JMM, and FAMF wrote the text. 29 (7): 807. Rasch JA, Bauer RT (2016) Reproductive pattern and sexual system of the nocturnal seagrass shrimp Ambidexter symmetricus (Decapoda: References Caridea: Processidae) in a Florida bay. Marine and Freshwater Abele LG (1972) A review of the genus Ambidexter (Crustacea: Research 67: 1141–1152. https://doi.org/10.1071/MF14159 Decapoda: Processidae) in Panama. Bulletin of Marine Science 22: Riul P, Rodrigues FMA, Xavier-Filho ES, Santos RG, Leonel RMV, 365–380. Christoffersen ML (2008) Macrocrustaceans from Ponta do Cabo Almeida AO, Bezerra LEA (2011) Nikoides schmitti Manning & Chace, Branco, João Pessoa, Paraíba, Brazil, the easternmost point of 1971 (Caridea: Processidae) in the South Atlantic Ocean, with an South America. Revista Nordestina de Biologia 19: 3–13. updated list and key for processid shrimps of Brazil. Zootaxa 2864: Ríus R, Carvacho A (1982) Caridean shrimps of the Gulf of California. 34–42. I. New records, with some remarks on amphiamerican distribution. Almeida AO, Boehs G, Araújo-Silva CL, Bezerra LEA (2012) Shallow- Pacific Science 36 (4): 459–465. water caridean shrimps from southern Bahia, Brazil, including Rubel, F, Kottek M (2010) Observed and projected climate shifts the first record of Synalpheus ul (Alpheidae) in the southwestern 1901–2100 depicted by world maps of the Köppen-Geiger Atlantic Ocean. Zootaxa 3347: 1–35. https://doi.org/10.11646/ climate classification. Meteorology 19: 135–141. https://doi. zootaxa.3905.1.3 org/10.1127/0941-2948/2010/0430 Moraes et al. | Ambidexter symmetricus: first record for Rio Grande do Norte, Brazil 543

Figure 2. Geographic distribution of Ambidexter symmetricus Manning & Chace, 1971 in Brazil. Location numbers are listed in Table 1. 544 Check List 14 (3)

Santos MAC, Coelho PA (1998a) Sazonalidade da ocorrência de crus- Coelho PA (2011) Marine and estuarine shrimps (Dendrobran- táceos decápodos no litoral de Jaboatão dos Guararapes, Pernam- chiata, Stenopodidea, and Caridea), of Pernambuco state (Brazil) buco – Brasil. Trabalhos Oceanográficos da Universidade Federal and northeastern brazilian oceanic islands. Atlântica, Rio Grande de Pernambuco 26 (1): 63–83. 33 (1): 33–63. https://doi.org/10.5088/atl. 2011.33.1.33 Santos MAC, Coelho PA (1998b) Camarões (Crustacea Decapoda) do Terossi M, Mantellato FL (2014) First zoeal stage of Processidae Litoral de Jaboatão dos Guararapes, Pernambuco – Brasil. Traba- (Decapoda, Caridea): review and new descriptions of Ambidexter lhos Oceanográficos da Universidade Federal de Pernambuco 26 symmetricus Manning and Chace 1971 and Processa fimbriata (1): 63–83. Manning and Chace 1971. Helgoland Marine Research 68: 483– Souza JAF, Schwamborn R, Barreto AV, Farias I D, Fernandes LMG, 489. https://doi.org/10.1007/s10152-014-0403-6